ARTICLE Received 12 Apr 2012 | Accepted 4 Sep 2012 | Published 9 Oct 2012 DOI: 10.1038/ncomms2111 Extreme binocular vision and a straight bill facilitate tool use in New Caledonian crows Jolyon Troscianko1, Auguste M.P. von Bayern2, Jackie Chappell1,*, Christian Rutz2,†,* & Graham R. Martin1,* Humans are expert tool users, who manipulate objects with dextrous hands and precise visual control. Surprisingly, morphological predispositions, or adaptations, for tool use have rarely been examined in non-human animals. New Caledonian crows Corvus moneduloides use their bills to craft complex tools from sticks, leaves and other materials, before inserting them into deadwood or vegetation to extract prey. Here we show that tool use in these birds is facilitated by an unusual visual-field topography and bill shape. Their visual field has substantially greater binocular overlap than that of any other bird species investigated to date, including six non- tool-using corvids. Furthermore, their unusually straight bill enables a stable grip on tools, and raises the tool tip into their visual field’s binocular sector. These features enable a degree of tool control that would be impossible in other corvids, despite their comparable cognitive abilities. To our knowledge, this is the first evidence for tool-use-related morphological features outside the hominin lineage. 1 School of Biosciences, University of Birmingham, Birmingham B15 2TT, UK. 2 Department of Zoology, University of Oxford, South Parks Road, Oxford OX1 3PS, UK. † Present address: School of Biology, University of St Andrews, Sir Harold Mitchell Building, St Andrews KY16 9TH, UK. *These authors are joint senior authors. Correspondence and requests for materials should be addressed to J.T. (email: [email protected]) or to C.R. (email: [email protected]). NATURE COMMUNICATIONS | 3:1110 | DOI: 10.1038/ncomms2111 | www.nature.com/naturecommunications © 2012 Macmillan Publishers Limited. All rights reserved. ARTICLE NatUre cOMMUNicatiONS | DOI: 10.1038/ncomms2111 ool-using animals must be able to hold tools firmly and guide and Table 1), using a well-established ophthalmoscopic reflex them accurately. Humans possess several morphological technique7. NC crows had a mean ( ± s.e.m.) maximum binocular Tfeatures that aid their precise handling and deployment of overlap of 61.5° ± 0.2 (n = 3), which is much greater (by between tools, including a powerful visual system for accurate relative depth 14.8° and 23.9°; see Table 1) than that observed in the five non- perception1, and hands with opposable thumbs for a secure grip2,3. tool-using Corvus species examined in this study, and a previously Comparatively few non-human animal species are known to use reported value for American crows C. brachyrhynchos8. This striking tools in the wild4, and it remains unknown whether any of them degree of binocularity appears to be at least partly due to unusually benefit from similar morphological predispositions or adaptations. large eye-movement amplitudes (Table 1). The average maximum New Caledonian crows Corvus moneduloides (‘NC crows’ here­ binocular field width of NC crows exceeded that of other Corvus after) use tools for extractive foraging5, exhibiting a remarkable species over 140° of elevation, spanning from the bill tip to behind degree of dexterity. Using their bills, these tropical birds craft com- the head (Fig. 1). plex tools from sticks, leaf edges and other materials, before insert- An exhaustive review of previously published material on avian ing them into deadwood or vegetation to ‘fish’ for invertebrate prey6. visual fields yielded comparative data for 46 bird species across 19 In this study, we show that NC crows present at least two unusual orders (Supplementary Table S1). NC crows exhibited consider- morphological features that combine to facilitate their use of tools: ably larger maximum binocular overlap than all other passerines extreme binocular vision and an uncharacteristically straight bill. (Corvus species excluded) and all non-passerines in this database Taken together, these adaptations enable a secure grip and accurate (Fig. 2, Table 1, Supplementary Table S1), exceeding the highest visual guidance of the tool, even when probing into narrow holes. species values by 10.5° and 13.5°, respectively. Results Visual control during tool deployment. To examine the hypoth- Visual-field topography. We measured visual-field parameters esis that the unusual visual-field topography of NC crows supports (monocular, binocular and cyclopean fields) and eye-movement their tool-use behaviour, we conducted behavioural experiments amplitudes in 18 alert subjects from 6 Corvus species (Figs 1 and 2 with three wild-caught subjects. Using a custom-built infrared NC crow 0 10 20 3040 Carrion crow 0 10 20 30 40 Jackdaw 0 10 20 3040 0 10 20 3040 0 10 20 3040 0 10 20 3040 Pied crow Raven Mean retinal field boundary Retinal field boundary (n=1) Rook Binocular sector +/– 1 s.e.m. of mean retinal field boundary Tool projection angle +/– 1 s.e.m. Line of the bill Figure 1 | Visual-field projections on orthographically viewed spheres for sixCorvus species. The diagrams use a conventional latitude and longitude coordinate system (with 10° intervals), aligned so that the bill tip is in line with the eyes in the horizontal plane, and the median sagittal plane of the skull (denoted by the white kite shapes). It should be imagined that the bird’s head is positioned at the centre of the transparent sphere, with the bill tip and field boundaries projected onto the surface of the sphere. Estimated tool-projection angles are plotted onto the spheres, to examine to what degree the six different species can potentially rely on visual feedback of tool-tip position during tool deployment. Only in the NC crow do the tool-projection angles fall completely within the binocular sector, such that the contralateral eye is able to see along the tool (cf. Fig. 4). NatUre cOMMUNicatiONS | 3:1110 | DOI: 10.1038/ncomms2111 | www.nature.com/naturecommunications © 2012 Macmillan Publishers Limited. All rights reserved. NATURE COMMUNICATIONS | DOI: 10.1038/ncomms2111 ARTICLE the cheek against which the tool is secured; Fig. 4b), which is better 60 positioned than the ipsilateral eye to maintain visual contact with the tool tip; meanwhile, the tool tip will lie closer to the central opti- cal axis of the ipsilateral eye (that is, further from the limits of the retina). When the aperture of the hole was experimentally reduced 50 in size, so that only one eye could see into the tube, our subjects pro- portionately increased the use of angled grips (for GLMM results, see above), which position both eyes equidistant to the line of the 40 lap (degrees) tool, bringing the eye that is ipsilateral during the angled grip closer er to the tool (Figs 3 and 4b). In interspersed control trials, where the ov tube had a visual aperture large enough for both eyes to see into, 30 but a small physical opening, our crows used an angled grip more frequently than a straight grip in comparison with the small aper- ture (GLMM: z = − 2.99, P = 0.003), although this was still a lower 20 proportion of angled grips than that observed for the large aperture (GLMM: z = − 4.37, P < 0.001). This shows that the visual properties of a hole alone are sufficient to determine the tool grip used by NC Maximum binocular crows while probing. 10 Taken together, our behavioural experiments suggest that, as visual hole apertures become smaller, NC crows shift their grip to bring the (formerly) ipsilateral eye closer to the tool, enabling 0 it to maintain visual contact with the tool tip. Further behavioural n w w testing would be necessary to establish whether NC crows are ow ow ow ve ines ines able to utilize their large binocular fields for stereoscopic depth kda Rook c Ra perception, which may be useful for gauging distances during tool on cr sser NC cro Ja ri ican cr 11 Pied cr deployment . Pa Car Amer Non-passer Bill shape and tool-projection angles. We next combined our vis- ual-field data with morphometric measurements, to assess whether Corvus spp. Species means any of our non-tool-using Corvus study species could, theoretically, achieve levels of physical and visual tool control similar to those Figure 2 | Maximum binocular overlap in tool-using NC crows and inferred for NC crows. Tools can be securely held in the bill in several non-tool-using control species. For the Corvus species, mean values are ways (Fig. 4b). In addition to the two principal modes described shown with s.e.m. (vertical bars) and 95% confidence intervals (shaded above, crows could hold stick tools perpendicular to the bill axis boxes), except for the pied crow (single data point) and the American crow (position 3 in Fig. 4b), so that the working tip of the tool can be (previously published mean value8); colour coding is the same as in positioned in a region covered by the visual field of the respective Fig. 1. For the samples of other passerine and non-passerine birds, ipsilateral eye. However, such a grip positions the line of the tool datapoints are (horizontally jittered) species values (means where further from the eye than an angled, or straight, grip (positions available; see Supplementary Table S1). Although the degree of 1 and 2 in Fig. 4b), making this grip less suitable for foraging in binocularity in non-tool-using Corvus species is similar to that of all other small holes (in Fig. 4b, an angled grip allows visual feedback from a passerines measured to date, NC crows represent a highly significant hole aperture approximately five times smaller than a perpendicu- outlier in this sample (see Table 1). Measurements for corvids were lar grip).